Instability of spring environmental conditions as a driver of biotic interactions and crustacean structuring in meteorite crater ponds (Morasko, Poland)

Although there are over 150 identified meteorite craters in the world, the occurrence of their aggregations is highly scattered (Hodge 2010). The studied meteorite crater ponds are one of the largest groups of meteorite craters in the world (Stankowski 2001). The literature concerning such specific ecosystems mainly refers to large lakes located in very deep craters of over 100 m depth, e.g. Lake Siljan in Sweden (Joakim 1989; Bengtsson, Malm 1997) or Lake Karakul in Tajikistan (Mishke et al. 2010). Some of them were found to be inhabited by new species or those that are rare in the region or country, for instance Lake Elgygytgyn, Russia (Cremer et al. 2005; Kharitonov, Genkal 2010). The previous investigation conducted within the crater ponds in Poland (Morasko) also revealed the presence of some zooplankton species which are not commonly observed in Poland (Kuczyńska-Kippen et al. 2013).

It was assumed that the fishless meteorite water bodies would be suitable sites to study interactions between micro-invertebrate groups. As the seasonal variation of environmental factors may have a great impact on zooplankton structure (Czerniawski, Domagała 2012; Simões et al. 2012; Ziadi et al. 2015), we restricted the study period to the spring season. Many studies are based on the summer zooplankton dynamics (e.g. Chojnacki, Wegleńska 1984; Havens 1991; Srichandan et al. 2014; Wang et al. 2015). However, the spring season is crucial for the development of zooplankton, especially in shallow water bodies which freeze to the bottom during winter and often dry up in the summer. Every year, these types of ponds create completely new niches for zooplankton communities, shortly after the ice melts. On the other hand, the spring season is characterized by instability of environmental factors – abiotic and biotic conditions change rapidly during the transitional period between winter and spring, i.e. from April to June, and in the transitional period between the spring and summer season. Moreover, the studied meteorite ponds are very shallow and supplied only by rainwater, therefore they may dry up during summer and often persist only in spring and autumn. Thus, we decided to conduct the study to observe the succession, development and dynamics of the crustacean community during the spring season.

Due to the temporary character of the studied water bodies, the crucial factor for crustacean survival may lay in the resting egg bank and the high hatching rate following dry periods. In accordance with the parthenogenetic reproduction, the cladoceran community develops faster than the copepod community (Ekvall, Hansson 2012). On the other hand, immature forms of Copepoda may be more abundant in comparison with cladoceran individuals (Lampert, Sommer 2001). Furthermore, the males’ occurrence helps cladocerans to survive under such unfavorable environmental conditions (Fryer 1968; Cáceres, Tessier 2004; Forró et al. 2008). The sexual eggs are much more resistant to harsh conditions than the parthenogenetic ones. Additionally, females hatched from sexual eggs supply their populations with new genetic material even after many years (Rybak, Błędzki 2010).

Vertebrate predators have a clear impact on the species composition and body size of crustaceans. Planktivorous fish feed on large Cladocera (e.g. from the Daphnidae family) more willingly than on smaller forms (e.g. from the Chydoridae family), therefore the dominance of small cladoceran species is characteristic of water bodies with fish. On the other hand, fishless water bodies are inhabited by large crustacean species which may be included in exploitative and interference competition with smaller zooplankters (Lampert et al. 2014). In the conditions where no vertebrate predators occur, invertebrate planktivores may take control over the crustacean community structure. Some invertebrates, such as the phantom midge Chaoborus larvae and adult copepods, are predators that consume cladocerans (Fryer 1957; Pastorok 1981; Gliwicz, Umana 1994; Castilho-Noll, Arcifa 2007). Contrary to fish predation, invertebrate predators are limited by their mouth gape size and hence they may have a stronger limiting effect, especially on small-sized crustaceans. While microcrustaceans are able to win the competition with mosquito larvae (Meyabeme Elono et al. 2010; Duquesne et al. 2011; Kroeger et al. 2014), shallow and fishless water bodies may be inhabited by other groups of potential competitors for Cladocera and Copepoda, e.g. ostracods.

Biotic interactions are a key factor in structuring the crustacean community. Therefore, we analyzed the relationships between invertebrates (including cladoceran males), predators and competitors in meteorite crater ponds of varying depth. We hypothesize that meteorite crater depth will significantly affect the invertebrate community structure. Moreover, the zooplankton competitors in the studied ponds as well as invertebrate predators will have different impacts on particular groups of crustaceans: small and large Cladocera, larvae and adult copepods.

The functioning of large and deep water bodies as well as the role of zooplankton has been the object of various research all over the world and over a relatively long period (e.g. Ikeda 1985; Jeppesen et al. 2011; Ejsmont-Karabin, Hutorowicz 2011). Although small water bodies have attracted the attention of scientists in the last two decades (e.g. Shurin 2000; Bhuiyan, Gupta 2007; Seminara et al. 2008; Czerniawski < Domagała 2013; Basińska et al. 2014), the knowledge of their role, the ecological mechanisms affecting their chemistry as well as the plant and animal communities that inhabit them is still insufficient, due to a great variety of pond types (Boix et al. 2012). This knowledge is insufficient especially in the case of rarer types of aquatic ecosystem, such as the meteorite craters presented in this study. The decomposition processes of organic matter (tree leaves) caused oxygen deficiencies and low pH, which together with the temporary character of the studied ponds resulted in a lack of fish, which makes those ecosystems suitable objects to study the biocenotic interactions in the invertebrate community.

The beginning of the spring season was characterized by low values of abundance and species richness for all the studied cladoceran groups, irrespective of the water body depth. This was a consequence of the specific character of small and shallow water bodies which freeze to the bottom during the winter season. Additionally, the location of ponds (forest surrounding, deep banks of craters) resulted in the shading of their surface which inhibited the spring increase in water temperature. Hence, the hatching rate of cladocerans from resting eggs was reduced after the ice had melted. The majority of Cladocera need a higher water temperature than that observed in April (mean 9-11°C) to build their community after the winter season. Vandekerkhove et al. (2005) suggest that the photoperiod is also important for the cladoceran development in the case of species richness as well as abundance. Moreover, we found a positive correlation in our study between the biocenotic parameters (abundance, species richness and diversity) of small and large cladocerans and water temperature, which is one of the crucial factors for the development of zooplankton communities in the early spring season.

After April, the total cladoceran abundance and species diversity increased, however, the trends were different in the case of small and large Cladocera. In general large cladocerans dominated over the small ones in all the studied ponds and periods. It is a typical phenomenon that large zooplankton organisms, e.g. representatives of Daphnia genus, often dominate in the absence of fish (Lampert et al. 2014), while in the case of water bodies with fish, the structuring often follows the direction of small forms of zooplankton (Havens, Beaver 2011; Iglesias et al. 2011; Vijverberg et al. 2014). Unlike the small cladocerans, the spring dynamics of large cladocerans was similar in every examined water body with the maximum values in May. Although the water temperature was higher in June than in May, the density and diversity of large cladocerans decreased toward the end of spring when the chlorophyll a concentration was the lowest, irrespective of the pond depth. Large cladocerans, e.g. from the Daphnia genus, are well known to be effective filtrators, which may reduce the phytoplankton development (Cottingham, Schindler 2000; Steiner 2002; Antilla et al. 2013). Therefore, the rapid increase in the abundance of large species, which was observed in May, might have led to phytoplankton food base depletion, which was also found in RDA results.

However, the abundance dynamics of small and large species was different: while high species richness and density of large cladocerans occurred mainly in May in all ponds, the distribution of small cladocerans varied in the case of pond depth. The May peak in the number and abundance of small cladoceran species was observed only in the medium ponds while in the remaining ponds (deep and shallow meteorite water bodies), the abundance of small cladocerans increased up to the June maximum. This suggests that other factors affect the dynamics of small and large cladocerans in meteorite crater ponds. Small species from the family Chydoridae are well adapted not only to obtain the food by filtration (Chydorus sphaericus) (Eyto, Irvine 2001), but also to scrape it from organic or inorganic substrata (Alonella genus) (Fryer 1968). Therefore, they may not be so sensitive to algae depletion as typical filtrators, such as e.g. Daphnia. On the other hand, due to their small size, they may be more susceptible to displacement by larger competitors such as daphnids, ostracods or mosquito larvae. The negative effect of competitors on their community structure was assumed to be due to low densities of small cladocerans during the whole study period. However, the multivariate analysis did not confirm this expectation. The competitors negatively correlated only with nauplii abundance. Furthermore, the food base conditions were positively correlated with the deepest pond where invertebrate predators were most abundant. Both size groups of Cladocera were characterized by lower species richness, diversity and density in DP. Many authors (Preissen, Young 2005; Jäger et al. 2011; Juračka et al. 2011) have found that invertebrate predators have a negative effect on cladoceran communities in fishless water bodies. However, the observed negative correlation of small and large cladocerans with predator density strongly suggests a lack of selective predation impact by Chaoborus and carnivorous copepods. This result also suggests that the spring dynamics of small and large cladocerans was more affected by predator-prey interactions than by competition.

Similarly to small and large cladoceran densities, the males of Cladocera were also most abundant in May. Their occurrence was the highest in the case of the shallowest pond (SP) and negatively correlated with a high oxygen concentration as well as with high pH of water. The lowest values of these water parameters (recorded in SP) could have been unfavorable for most of the cladoceran taxa and could have been the reason for the high abundance of the cladoceran males. Forró et al. (2008) established that a high contribution of males helps the community of cladocerans to survive and hence proves their resistance to harsh habitat conditions (Fryer 1968; Cáceres, Tessier 2004). This explain why cladoceran males usually occur in the autumn (Jankowski, Straile 2004; Nevalainen, Sarmaja-Korjonen 2008; Martin et al. 2014). However, the unfavorable conditions, observed in the studied meteorite ponds, resulted in the presence of an abundant community of Cladocera males in the spring. The abundance of cladoceran females was not negatively correlated with the conditions of low oxygen concentration. In general, they were represented by daphnids, which are known to be well adapted to unfavorable oxygen conditions through hemoglobin production. Even though it is connected with high metabolic costs, it enables them to survive in conditions of oxygen depletion, because transport of oxygen by hemoglobin is more efficient compare to hemocyanin (Fox 1948; Green 1956; Pirow et al. 2001).

Contrary to the cladoceran community, copepod species composition was characterized by minor spring fluctuations in each of the studied pond and revealed different relations to environmental factors. The number of Copepoda species did not depend on a temperature increase. Many of them are eurythermal. However, their adult forms are usually more frequently observed in cold seasons (including early spring months) than in the summer (Rybak, Błędzki 2010; Lampert, Sommer 2001).

Adult copepod species, which dominated during the study period (Cyclops vicinus and Megacyclops viridis), are referred to in the literature as often observed in shallow ponds or littoral zones of lakes (Rybak, Błędzki 2010; Kumar et al. 2010; Aygen 2011). Therefore, they showed a positive correlation with the shallowest meteorite water body, even though this small reservoir was the most susceptible to drying in comparison with the deeper ones. However, the drought periods occur in summer, which is a diapause time for many of the observed copepod species (e.g. C. vicinus and M. viridis), therefore they are able to survive those dry periods (Rybak, Błędzki 2010). Moreover, the number and diversity of adult copepod species were favored by a higher content of biogenic substance, such as phosphates and nitrates. These compounds are mainly allochthonous in ponds supplied only by rainwater, so the biogenic substances are released in the process of decomposition of tree leaves on the pond bottom (Lampert, Sommer 2001; Sobczyński, Joniak 2009). These kinds of sediments can be an additional habitat for copepods as well as for other groups of organisms, such as bacteria, ciliates and ostracods which can also make up a supplementary food for some copepods.

The abundance of copepods was strongly dependent on the density of larvae, which usually reached ca. 95% of the total copepod abundance. In the case of the investigated meteor craters, Copepoda abundance was significantly higher than the cladoceran abundance. The high growth rate of copepods in the spring season may be connected with their ability to quickly colonize new ecosystems. On the other hand, the cladoceran resting egg bank may be a very important factor affecting the spring community structure of invertebrates. While drying or freezing of the water column may prevent adult individuals from surviving (Frisch, Green 2007), resting eggs can survive under these conditions and supply their population with new genetic material after the harsh conditions (Rybak, Błędzki 2010). Therefore, sexual eggs are important to cladoceran communities, especially in temporary water bodies. Cladocerans may also rapidly colonize ecosystems in the spring season, although they need a higher water temperature to develop quickly, compared to copepods (Rybak, Błędzki 2010). Thus, a seasonal segregation of both groups of crustaceans was observed as an effect of different life cycles of copepods and cladocerans as well as of the dependence of the Cladocera development on a high water temperature.

The abundance of copepods was not affected by predators. Nauplii and early copepodite stages are characterized by a small body size, therefore they can potentially be preyed upon by Chaoborus larvae. However, the fast swimming strategy of Copepoda and swift and rapid escape may prevent the success of predators (Reissen et al. 1984; Kiørboe et al. 2010). This suggests that despite the well-developed ability of copepod larvae to escape, invertebrate predators preferred to feed on cladocerans.

Despite the fact that the studied meteorite crater ponds were of the same origin and located in the same catchment area, and despite a small distance between the ponds, the spring dynamics of zooplankton was distinct different in particular water bodies. The spring succession of small cladocerans was modified by a pond depth, contrary to the dynamics of large cladocerans. The fishless character of the analyzed ponds resulted in the co-occurrence of small and large cladocerans as well as in a strong impact from invertebrate predators (phantom midge Chaoborus larvae and adult copepods) on their community structure. A similar effect of invertebrate predators on both size groups of Cladocera suggests the lack of their feeding selectivity. Moreover, copepod larvae were negatively affected by high competitor abundance (Aedes communis and ostracods).

The meteorite crate ponds were characterized by a low water level and oxygen depletions. Those unfavorable abiotic conditions resulted in the high density of Cladocera males during the spring season. Moreover, cladocerans from the genus Daphnia produced hemoglobin, which better transports oxygen in the organism than hemocyanin, so they were not sensitive to oxygen deficiencies.